Molecular piracy: Manipulation of the ubiquitin system by Kaposi's sarcoma-associated herpesvirus

Reviews in Medical Virology

Volumn 17, Issue 6, 2007, Pages 405-422

  Fujimuro, Masahiro ^a   Hayward, S Diane ^b   Yokosawa, Hideyoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; UBIQUITIN; WNT PROTEIN;

CELL CYCLE PROGRESSION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; ENDOCYTOSIS; HUMAN HERPESVIRUS 8; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW; VIRUS CARCINOGENESIS; VIRUS INTERFERENCE;

CARRIER PROTEINS; CELL CYCLE PROTEINS; HERPESVIRUS 8, HUMAN; HUMANS; SARCOMA, KAPOSI;

EID: 36348946252     PISSN: 10529276     EISSN: None     Source Type: Journal    
DOI: 10.1002/rmv.549     Document Type: Review

References (147)

1. Chang Y, Cesarman E, Pessin MS, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposis sarcoma. Science 1994; 266: 1865-1869.
2. Russo JJ, Bohenzky RA, Chein M-C, et al. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA 1996; 93: 14862-14867.
3. Ablashi DV, Chatlynne LG, Whitman JE Jr, et al. Spectrum of Kaposis sarcoma-associated herpesvirus, or human herpesvirus 8, diseases. Clin Microbiol Rev 2002; 15: 439-464.
4. Schulz TF. The pleiotropic effects of Kaposi's sarcoma herpesvirus. J Pathol 2006; 208: 187-198.
5. Dittmer D, Lagunoff M, Renne R, et al. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 1998; 72: 8309-8315.
6. Ballestas ME, Chatis PA, Kaye KM. Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 1999; 284: 641-644.
7. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, et al. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 2006; 311: 856-861.
8. Hu J, Garber AC, Renne R. The latency-associated nuclear antigen of Kaposis sarcoma-associated herpesvirus supports latent DNA replication in dividing cells. J Virol 2002; 76: 11677-11687.
9. Grundhoff A, Ganem D. The latency-associated nuclear antigen of Kaposis sarcoma-associated herpesvirus permits replication of terminal repeat-containing plasmids. J Virol 2003; 77: 2779-2783.
10. Radkov SA, Kellam P, Boshoff C. The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene H-ras transforms primary rat cells. Nat Med 2000; 6: 1121-1127.
11. Friborg JJ, Kong W, Hottiger MO, et al. p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 1999; 402: 889-894.
12. Fujimuro M, Hayward SD. Manipulation of glycogen-synthase kinase-3 activity in KSHV-associated cancers. J Mol Med 2004; 82: 223-231.
13. Hayward SD, Liu J, Fujimuro M. Notch and Wnt signaling: mimicry and manipulation by 7 herpesviruses. Sci STKE 2006; 335: re4.
14. Moore PS, Chang Y. Molecular virology of Kaposis sarcoma-associated herpesvirus. Philos Trans R Soc Lond B Biol Sci 2001; 356: 499-516.
15. Choi J, Means RE, Damania B, et al. Molecular piracy of Kaposis sarcoma associated herpesvirus. Cytokine Growth Factor Rev 2001; 12: 245-257.
16. Nicholas J, Zong JC, Alcendor DJ, et al. Novel organization features, captured cellular genes and strain variability within the genome of KSHV/HHV8. J Natl Cancer Inst Monogr 1998; 23: 79-88.
17. Jenner RG, Boshoff C. The molecular pathology of Kaposis sarcoma-associated herpesvirus. Biochim Biophys Acta 2002; 1602: 1-22.
18. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2001; 82: 373-428.
19. Hicke L. Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2001; 2: 195-201.
20. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 2005; 6: 79-87.
21. Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001; 70: 503-533.
22. Banks L, Pim D, Thomas M. Viruses and the 26S proteasome: hacking into destruction. Trends Biochem Sci 2003; 28: 452-459.
23. Bieniasz PD. Late budding domains and host proteins in enveloped virus release. Virology 2006; 344: 55-63.
24. Shackelford J, Pagano JS. Targeting of host-cell ubiquitin pathways by viruses. Essays Biochem 2005; 41: 139-156.
25. Gao G, Luo H. The ubiquitin-proteasome pathway in viral infections. Can J Physiol Pharmacol 2006; 84: 5-14.
26. Scheffner M, Whitaker NJ. Human papillomavirus-induced carcinogenesis and the ubiquitinproteasome system. Semin Cancer Biol 2003; 13: 59-67.
27. Sulea T, Lindner HA, Menard R. Structural aspects of recently discovered viral deubiquitinating activities. Biol Chem 2006; 387: 853-862.
28. Shackelford J, Pagano JS. Tumor viruses and cell signalling pathways: deubiquitination versus ubiquitination. Mol Cell Biol 2004; 24: 5089-5093.
29. Nijman SM, Luna-Vargas MP, Velds A, et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005; 123: 773-786.
30. Voges D, Zwickl P, Baumeister W. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 1999; 68: 1015-1068.
31. Kohler A, Cascio P, Leggett DS, et al. The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Mol Cell 2001; 7: 1143-1152.
32. Scheffner M, Werness BA, Huibregtse JM, et al. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990; 63: 1129-1136.
33. Jackson PK, Eldridge AG, Freed E, et al. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol 2000; 10: 429-439.
34. Nakayama KI, Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 2006; 6: 369-381.
35. Deshaies RJ. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 1999; 15: 435-467.
36. Winston JT, Strack P, Beer-Romero P, et al. The SCF(β-TRCP)-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev 1999; 13: 270-283.
37. Hao B, Oehlmann S, Sowa ME, et al. Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol Cell 2007; 26: 131-143.
38. Michael D, Oren M. The p53 and Mdm2 families in cancer. Curr Opin Genet Dev 2002; 12: 53-59.
39. Querido E, Blanchette P, Yan Q, et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev 2001; 15: 3104-3117.
40. Chiu YL, Greene WC. Multifaceted antiviral actions of APOBEC3 cytidine deaminases. Trends Immunol 2006; 27: 291-297.
41. Ehrlich ES, Yu XF. Lentiviral Vif: viral hijacker of the ubiquitin-proteasome system. Int J Hematol 2006; 83: 208-212.
42. Boutell C, Sadis S, Everett RD. Herpes simplex virus type 1 immediate early protein ICPO and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J Virol 2002; 76: 841-850.
43. Chelbi-Alix MK, de The H. Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 1999; 18: 935-941.
44. Van Sant C, Hagglund R, Lopez P, et al. The infected cell protein 0 of herpes simplex virus 1 dynamically interacts with proteasomes, binds and activates the cdc34 E2 ubiquitin-conjugating enzyme, and possesses in vitro E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 2001; 98: 8815-8820.
45. Everett RD, Meredith M, Orr A, et al. A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J 1997; 16: 1519-1530.
46. Holowaty MN, Frappier L, HAUSP/USP7 as an Epstein-Barr virus target. Biochem Soc Trans 2004; 32: 731-732.
47. Li M, Chen D, Shiloh A, et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilisation. Nature 2002; 416: 648-653.
48. Canning M, Boutell C, Parkinson J, et al. A RING finger ubiquitin ligase is protected from autocatalyzed ubiquitination and degradation by binding to ubiquitin-specific protease USP7. J Biol Chem 2004; 279: 38160-38168.
49. Coscoy L, Ganem D. PHD domains and E3 ubiquitin ligases: viruses make the connection. Trends Cell Biol 2003; 13: 7-12.
50. Ohmura-Hoshino M, Goto E, Matsuki Y, et al. A novel family of membrane-bound E3 ubiquitin ligases. J Biochem (Tokyo) 2006; 140: 147-154.
51. Barry M, Früh K. Viral modulators of cullin RING ubiquitin ligases: culling the host defense. Sci STKE 2006; 335: pe21.
52. Yu Y, Wang SE, Hayward GS. The KSHV immediate early transcription factor RTA encodes ubiquitin E3 ligase activity that targets IRF7 for proteosome-mediated degradation. Immunity 2005; 22: 59-70.
53. 5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumour suppressors. PLoS Pathog 2006; 2: e116.
54. Kamura T, Maenaka K, Kotoshiba S, et al. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev 2004; 18: 3055-3065.
55. Kamura T, Sato S, Iwai K, et al. Activation of HIF1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumour suppressor complex. Proc Natl Acad Sci USA 2000; 97: 10430-10435.
56. Ohh M, Park CW, Ivan M, et al. Ubiquitination of hypoxia-inducible factor requires direct binding to the β-domain of the von Hippel-Lindau protein. Nat Cell Biol 2000; 2: 423-427.
57. Haque M, Wang V, Davis DA, et al. Genetic organization and hypoxic activation of the Kaposi's sarcoma-associated herpesvirus ORF34-37 gene cluster. J Virol 2006; 80: 7037-7051.
58. Sun Y, Huang PL, Li JJ, et al. Anti-HIV agent MAP30 modulates the expression profile of viral and cellular genes for proliferation and apoptosis in AIDS-related lymphoma cells infected with Kaposi's sarcoma-associated virus. Biochem Biophys Res Commun 2001; 287: 983-994.
59. Sarek G, Kurki S, Enback J, et al. Reactivation of the p53 pathway as a treatment modality for KSHV-induced lymphomas. J Clin Invest 2007; 117: 1019-1028.
60. Petre CE, Sin SH, Dittmer DP. Functional p53 signalling in Kaposi's sarcoma-associated herpesvirus lymphomas: implications for therapy. J Virol 2007; 81: 1912-1922.
61. Chen ZJ. Ubiquitin signalling in the NF-κB pathway. Nat Cell Biol 2005; 7: 758-765.
62. Hiscott J, Nguyen TL, Arguello M, et al. Manipulation of the nuclear factor-κB pathway and the innate immune response by viruses. Oncogene 2006; 25: 6844-6867.
63. Brinkmann MM, Schulz TF. Regulation of intracellular signalling by the terminal membrane proteins of members of the Gammaherpesvirinae. J Gen Virol 2006; 87: 1047-1074.
64. Thome M, Schneider P, Hofmann K, et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 1997; 386: 517-521.
65. Chaudhary PM, Jasmin A, Eby MT, et al. Modulation of the NF-κB pathway by virally encoded death effector domains-containing proteins. Oncogene 1999; 18: 5738-5746.
66. Matta H, Chaudhary PM. Activation of alternative NF-κB pathway by human herpesvirus 8-encoded Fas-associated death domain-like IL-1β-converting enzyme inhibitory protein (vFLIP). Proc Natl Acad Sci USA 2004; 101: 9399-9404.
67. Chugh P, Matta H, Schamus S, et al. Constitutive NF-κB activation, normal Fas-induced apoptosis, and increased incidence of lymphoma in human herpes virus 8 K13 transgenic mice. Proc Natl Acad Sci USA 2005; 102: 12885-12890.
68. Liu L, Eby MT, Rathore N, et al. The human herpesvirus 8-encoded viral FLICE inhibitory protein physically associates with and persistently activates the IKB kinase complex. J Biol Chem 2002; 277: 13745-13751.
69. Field N, Low W, Daniels M, et al. KSHV vFLIP binds to IKK-7 to activate IKK. J Cell Sci 2003; 116: 3721-3728.
70. Guasparri I, Wu H, Cesarman E. The KSHV oncoprotein vFLIP contains a TRAF-interacting motif and requires TRAF2 and TRAF3 for signalling. EMBO Rep 2006; 7: 114-119.
71. An J, Sun Y, Sun R, et al. Kaposi's sarcoma-associated herpesvirus encoded vFLIP induces cellular IL-6 expression: the role of the NF-κB and JNK/AP1 pathways. Oncogene 2003; 22: 3371-3385.
72. Guasparri I, Keller SA, Cesarman E. KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 2004; 199: 993-1003.
73. Keller SA, Schattner EJ, Cesarman E, Inhibition of NF-κB induces apoptosis of KSHV-infected primary effusion lymphoma cells. Blood 2000; 96: 2537-2542.
74. Brown HJ, Song MJ, Deng H, et al. NF-κB inhibits gammaherpesvirus lytic replication. J Virol 2003; 77: 8532-8540.
75. Sun Q, Zachariah S, Chaudhary PM. The human herpes virus 8-encoded viral FLICE-inhibitory protein induces cellular transformation via NF-κB activation. J Biol Chem 2003; 278: 52437-52445.
76. Brinkmann MM, Glenn M, Rainbow L, et al. Activation of mitogen-activated protein kinase and NF-κB pathways by a Kaposi's sarcoma-associated herpesvirus K15 membrane protein. J Virol 2003; 77: 9346-9358.
77. Schwarz M, Murphy PM. Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor constitutively activates NF-κB and induces proinflammatory cytokine and chemokine production via a C-terminal signalling determinant. J Immunol 2001; 167: 505-513.
78. Pati S, Cavrois M, Guo HG, et al. Activation of NF-κB by the human herpesvirus 8 chemokine receptor ORF74: evidence for a paracrine model of Kaposi's sarcoma pathogenesis. J Virol 2001; 75: 8660-8673.
79. Lee H, Veazey R, Williams K, et al. Deregulation of cell growth by the K1 gene of Kaposi's sarcoma-associated herpesvirus. Nat Med 1998; 4: 435-440.
80. Prakash O, Tang ZY, Peng X, et al. Tumorigenesis and aberrant signalling in transgenic mice expressing the human herpesvirus-8 K1 gene. J Natl Cancer Inst 2002; 94: 926-935.
81. Wang HW, Sharp TV, Koumi A, et al. Characterization of an anti-apoptotic glycoprotein encoded by Kaposi's sarcoma-associated herpesvirus which resembles a spliced variant of human survivin. EMBO J 2002; 21: 2602-2615.
82. Feng P, Scott CW, Cho NH, et al. Kaposi's sarcoma-associated herpesvirus K7 protein targets a ubiquitin-like/ubiquitin-associated domain-containing protein to promote protein degradation. Mol Cell Biol 2004; 24: 3938-3948.
83. Seo T, Park J, Lim C, et al. Inhibition of nuclear factor κB activity by viral interferon regulatory factor 3 of Kaposi's sarcoma-associated herpesvirus. Oncogene 2004; 23: 6146-6155.
84. Jarviluoma A, Ojala PM. Cell signalling pathways engaged by KSHV. Biochim Biophys Acta 2006; 1766: 140-158.
85. Direkze S, Laman H. Regulation of growth signalling and cell cycle by Kaposi's sarcoma-associated herpesvirus genes. Int J Exp Patho 2004; 85: 305-319.
86. Mittnacht S, Boshoff C. Viral cyclins. Rev Med Virol 2000; 10: 175-184.
87. Chang Y, Moore PS, Talbot SJ, et al. Cyclin encoded by KS herpesvirus. Nature 1996; 382: 410.
88. Godden-Kent D, Talbot SJ, Boshoff C, et al. The cyclin encoded by Kaposi's sarcoma-associated herpesvirus stimulates cdk6 to phosphorylate the retinoblastoma protein and histone H1. J Virol 1997; 71: 4193-1198.
89. Swanton C, Mann DJ, Fleckenstein B, et al. Herpes viral cyclin/Cdk6 complexes evade inhibition by CDK inhibitor proteins. Nature 1997; 390: 184-187.
90. Ellis M, Chew YP, Fallis L, et al. Degradation of p27 (Kip) cdk inhibitor triggered by Kaposi's sarcoma virus cyclin-cdk6 complex. EMBO J 1999; 18: 644-653.
91. Mann DJ, Child ES, Swanton C, et al. Modulation of p27 (Kip1) levels by the cyclin encoded by Kaposi's sarcoma-associated herpesvirus. EMBO J 1999; 18: 654-663.
92. Jarviluoma A, Koopal S, Rasanen S, et al. KSHV viral cyclin binds to p27KIP1 in primary effusion lymphomas. Blood 2004; 104: 3349-3354.
93. Laman H, Coverly D, Krude T, et al. Viral cyclin-cylin dependent kinase 6 complexes initiate nuclear DNA replication. Mol Cell Biol 2001; 21: 624-635.
94. Ojala PM, Yamamoto K, Castanos-Velez. E, et al. The apoptotic v-cyclin-CDK6 complex phosphorylates and inactivates Bcl-2. Nat Cell Biol 2000; 2: 819-825.
95. KIP1 through Ser10 and Thr187 phosphorylation in proliferating primary effusion lymphomas. Blood 2006; 107: 725-732.
96. Kamura T, Hara T, Matsumoto M, et al. Cytoplasmic ubiquitin ligase KPC regulates proteolysis of p27(Kip1) at G1 phase. Nat Cell Biol 2004; 6: 1229-1235.
97. Kimelman D, Xu W. β-catenin destruction complex: insights and questions from a structural perspective. Oncogene 2006; 25: 7482-7491.
98. Willert K, Jones KA. Wnt signalling: is the party in the nucleus? Genes Dev 2006; 20: 1394-1404.
99. Clevers H. Wnt/β-catenin signalling in development and disease. Cell 2006; 127: 469-180.
100. Hoppler S, Kavanagh CL. Wnt signalling: variety at the core. J Cell Sci 2007; 120: 385-393.
101. Segditsas S, Tomlinson I. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 2006; 25: 7531-7537.
102. Clements WM, Wang J, Sarnaik A, et al. β-Catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer. Cancer Res 2002; 62: 3503-3506.
103. Fujimuro M, Wu FY, apRhys C, et al. A novel viral mechanism for dysregulation of β-catenin in Kaposis sarcoma-associated herpesvirus latency. Nat Med 2003; 9: 300-306.
104. Fujimuro M, Hayward SD. The latency-associated nuclear antigen of Kaposis sarcoma-associated herpesvirus manipulates the activity of glycogen synthase kinase-3β. J Virol 2003; 77: 8019-8030.
105. Bijur GN, Jope RS. Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3β. J Biol Chem 2001; 276: 37436-37442.
106. Diehl JA, Cheng M, Roussel MF, et al. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998; 12: 3499-3511.
107. Webster MT, Rozycka M, Sara E, et al. Sequence variants of the axin gene in breast, colon, and other cancers: an analysis of mutations that interfere with GSK3 binding. Genes Chromosomes Cancer 2000; 28: 443-153.
108. Fujimuro M, Liu J, Zhu J, et al. Regulation of the interaction between glycogen synthase kinase 3 and the Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen. J Virol 2005; 79: 10429-10441.
109. Ding Q, Xia W, Liu JC, et al. Erk associates with and primes GSK-3β for its inactivation resulting in upregulation of β-catenin. Mol Cell 2005; 19: 159-170.
110. Liu J, Martin H, Shamay M, et al. Kaposi's sarcoma-associated herpesvirus LANA protein downregulates nuclear glycogen synthase kinase 3 activity and consequently blocks differentiation. J Virol 2007; 81: 4722-1731.
111. Bubman D, Guasparri I, Cesarman E. Deregulation of c-Myc in primary effusion lymphoma by Kaposi's sarcoma herpesvirus latency-associated nuclear antigen. Oncogene 2007; 26: 4979-4986.
112. Liu J, Martin HJ, Liao G, et al. The Kaposi sarcoma associated herpesvirus LANA protein stabilizes and activates c-Myc. J Virol, in press. DOI: 10.1128/JVI.00804-07.
113. Morrison JA, Gulley ML, Pathmanathan R, et al. Differential signalling pathways are activated in the Epstein-Barr virus-associated malignancies nasopharyngeal carcinoma and Hodgkin lymphoma. Cancer Res 2004; 64: 5251-5260.
114. Everly DN Jr, Kusano S, Raab-Traub N. Accumulation of cytoplasmic β-catenin and nuclear glycogen synthase kinase 3β in Epstein-Barr virus-infected cells. J Virol 2004; 78: 11648-11655.
115. Jang KL, Shackelford J, Seo SY, et al. Up-regulation of β-catenin by a viral oncogene correlates with inhibition of the seven in absentia homolog 1 in B lymphoma cells. Proc Natl Acad Sci USA 2005; 102: 18431-18436.
116. Ovaa H, Kessler BM, Rolen U, et al. Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells. Proc Natl Acad Sci USA 2004; 101: 2253-2258.
117. Shackelford J, Maier C, Pagano JS. Epstein-Barr virus activates β-catenin in type III latently infected B lymphocyte lines: association with deubiquitinating enzymes. Proc Natl Acad Sci USA 2003; 100: 15572-15576.
118. Liu J, Stevens J, Rote CA, et al. Siah-1 mediates a novel β-catenin degradation pathway linking p53 to the adenomatous polyposis coli protein. Mol Cell 2001; 7: 927-936.
119. Matsuzawa SI, Reed JC. Siah-1, SIP, and Ebi collaborate in a novel pathway for β-catenin degradation linked to p53 responses. Mol Cell 2001; 7: 915-926.
120. Hill A, Jugovic P, York I, et al. Herpes simplex virus turns off the TAP to evade host immunity. Nature 1995; 375: 411-115.
121. Lankat-Buttgereit B, Tampe R. The transporter associated with antigen processing: function and implications in human diseases. Physiol Rev 2002; 82: 187-204.
122. Lilley BN, Ploegh HL. Viral modulation of antigen presentation: manipulation of cellular targets in the ER and beyond. Immunol Rev 2005; 207: 126-144.
123. Gilbert MJ, Riddel SR, Plachter B, et al. Cytomegalovirus selectivity blocks antigen processing and presentation of its immediate-early gene product. Nature 1996; 383: 720-722.
124. Keating S, Prince S, Jones M, et al. The lytic cycle of Epstein-Barr virus is associated with decreased expression of cell surface major histocompatibility complex class I and class II molecules. J Virol 2002; 76: 8179-8188.
125. Levitskaya J, Coram M, Levitsky V, et al. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 1995; 375: 685-688.
126. Levitskaya J, Shapiro A, Leonchiks A, et al. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci USA 1997; 94: 12616-12621.
127. + T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity 1997; 7: 791-802.
128. Yin Y, Manoury B, Fahraeus R. Self-inhibition of synthesis and antigen presentation by Epstein-Barr virus-encoded EBNAl. Science 2003; 301: 1371-1374.
129. Heessen S, Leonchiks A, Issaeva N, et al. Functional p53 chimeras containing the Epstein-Barr virus Gly-Ala repeat are protected from Mdm2-and HPV-E6-induced proteolysis. Proc Natl Acad Sci USA 2002; 99: 1532-1537.
130. Ossevoort M, Zaldumbide A, Te Velthuis AJ, et al. The nested open reading frame in the Epstein-Barr virus nuclear antigen-1 mRNA encodes a protein capable of inhibiting antigen presentation in cis. Mol Immunol 2007; 44: 3588-3596.
131. Zaldumbide A, Ossevoort M, Wiertz EJ, et al. In cis inhibition of antigen processing by the latency-associated nuclear antigen I of Kaposi sarcoma herpes virus. Mol Immunol 2007; 44: 1352-1360.
132. Rezaee SA, Cunningham C, Davison AJ, et al. Kaposi's sarcoma-associated herpesvirus immune modulation: an overview. J Gen Virol 2006; 87: 1781-1804.
133. Moore PS, Chang Y. Kaposi's sarcoma-associated herpesvirus immunoevasion and tumorigenesis: two sides of the same coin? Annu Rev Microbiol 2003; 57: 609-639.
134. Coscoy L, Ganem D. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc Natl Acad Sci USA 2000; 97: 8051-8056.
135. Ishido S, Wang C, Lee BS, et al. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 2000; 74: 5300-5309.
136. Brander C, Suscovich T, Lee Y, et al. Impaired CTL recognition of cells latently infected with Kaposi's sarcoma-associated herpes virus. J Immunol 2000; 165: 2077-2083.
137. Nicholas J, Ruvolo V, Zong J, et al. A single 13-kilobase divergent locus in the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) genome contains nine open reading frames that are homologous to or related to cellular proteins. J Virol 1997; 71: 1963-1974.
138. Coscoy L, Ganem D. A viral protein that selectively downregulates ICAM-1 and B7-2 and modulates T cell costimulation. J Clin Invest 2001; 107: 1599-1606.
139. Ishido S, Choi JK, Lee BS, et al. Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein. Immunity 2000; 13: 365-374.
140. Coscoy L, Sanchez DJ, Ganem D. A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J Cell Biol 2001; 155: 1265-1273.
141. Sanchez DJ, Gumperz JE, Ganem D. Regulation of CDId expression and function by a herpes-virus infection. J Clin Invest 2005; 115: 1369-1378.
142. Duncan LM, Piper S, Dodd RB, et al. Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J 2006; 25: 1635-1645.
143. Cadwell K, Coscoy L. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 2005; 309: 127-130.
144. Stevenson PG, Efstathiou S, Doherty PC, et al. Inhibition of MHC class I-restricted antigen presentation by γ2-herpesviruses. Proc Natl Acad Sci USA 2000; 97: 8455-8460.
145. + T cells aids amplification of a latent 7-herpesvirus. Nat Immunol 2002; 3: 733-740.
146. Brown HJ, McBride WH, Zack JA, et al. Prostratin and bortezomib are novel inducers of latent Kaposi's sarcoma-associated herpesvirus. Antivir Ther 2005; 10: 745-51.
147. Matta H, Chaudhary PM. The proteasome inhibitor bortezomib (PS-341) inhibits growth and induces apoptosis in primary effusion lymphoma cells. Cancer Biol Ther 2005; 4: 77-82.